Tropical Natural History 20(1): 95-103, April 2020 2020 by Chulalongkorn University

Short Note Social Behavior Displayed by the Green Pit Viper Trimeresurus (Cryptelytrops) macrops

CURT H. BARNES1*, WILLIAM FARREN2, COLIN T. STRINE1 AND PONGTHEP SUWANWAREE1

1Suranaree University of Technology, Nakhon Ratchasima, THAILAND 2Sakaerat Conservation and Education Team, Sakaerat Environmental Research Station, Nakhon Ratchasima, THAILAND * Corresponding Author: Curt H. Barnes ([email protected]) Received: 18 March 2019; Accepted: 11 November 2019

Study of behavior and sociality has sidewinder (C. cerastes) rattlesnakes to historically been well-represented in non- evaluate social behavior (summarized5,10). squamate amniotic organisms1-3. Such study Investigation of viper behavior in the tropics with squamates (lizards, , and has progressed little past spatial ecology. amphisbaenians) is still in the infancy stage Arboreal vipers are among the least studied however, especially regarding snakes4,5. snakes because of limiting factors such as While more complex and visible social body size and challenging habitats11. Recent systems may be observed for mammals and study of green pit vipers (Trimeresurus birds, understanding of seemingly simpler spp.) suggests moderate home range overlap behavior and sociality displayed by snakes between conspecific females, as well as may provide valuable insight from which interspecies overlap in males12. complexity may be derived5. Behaviors related to sexual activity, such Reliable and comprehensive knowledge as male combat, courtship, and mating, are is essential if behavioral ecology is to serve considered as evidence of social systems13. as an effective conservation tool6. Snakes also interact and aggregate with Contesting the traditional perception that the conspecifics for reasons other than snake clade completely lacks complex and procreation-even before they are born- noteworthy social behavior has been a aggregations of gravid females in several considerable challenge7,8. Viper home rattlesnake , a form of parental care ranges in temperate regions frequently (> 50 species of > 30 genera), and overlap with conspecifics and limited cooperative hunting in sea snakes, all interactions between species were evidence snakes are an overlooked source of infrequently reported until fairly recently9. social behavior8. To date, most behavioral and social study of We present observations of social wild snakes has been conducted with interactions of wild adult big-eyed pit vipers temperate climate vipers, particularly (Trimeresurus (Cryptelytrops) macrops14) at rattlesnakes. Camera technology has ambush sites within the Sakaerat Biosphere recently been utilized with considerable Reserve (SBR) in northeast Thailand. Like success on red diamond (Crotalus ruber), most other green pit vipers, T. macrops northern pacific (C. oreganus), timber (C. exhibits profound sexual dimorphism both horridus), Arizona black (C. cerberus), and in size and coloration15. Male T. macrops TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 96 display a vibrant white “racing stripe” male (SVL = 424 mm, mass = 24.2 g, Table (postocular stripe) above each eye, which 1) at the transition zone study site in our females lack, and could play a role in investigation. signaling of body condition. Females are Field videography: We set Bushnell trail significantly larger morphologically, not cameras Model X-8 (model #119327, f/3, only in body mass and snout-vent length but exposure time 1/20 sec, ISO 100, 35mm also in head width and length. focal length, infrared night capability) and Study site and : Our observations Trophy Cam (model #119636C, f/2.8, were part of a larger project looking at green exposure time 1/20 sec, ISO 100, 35mm pit viper behavior, spatial ecology, and focal length, infrared night capability) habitat selection within the Sakaerat approximately 1-3 m from focal adult green Biosphere Reserve in northeast Thailand. At pit vipers after a minimum 2 week recovery our sites, we opportunistically captured period from latest capture (Fig. 1). The vipers during visual searches after dark and camera interval was one minute with one or then recorded morphometrics (snout-vent three consecutive photographs taken each length [SVL] and body mass) the following minute. Care was taken when placing day with an acrylic tube and isoflurane cameras not to disturb vipers or anesthesia described by Wilkinson (2014)16. considerably alter natural behavior and We sexed each individual under anesthesia. habitat, and we did not use recordings in We gently palpated for the presence of which vipers abandoned ambush or resting vitellogenic follicles and embryos under sites within an hour of setting cameras for anesthesia, if present we considered them to analyses. be “gravid” and if not then “not gravid.” Ethology: We specifically looked at Radio transmitters (1.8 g, Holohil BD-2T interactions between focal T. macrops and and BD2-THX) were implanted in adult pit conspecifics which occurred on the cameras vipers deemed large enough and in good while pit vipers were ambushing. We condition (transmitter < 5% of body mass) defined ambush behavior as stationary following 17,18. foraging, coiled with the head set in a ready- We radiotracked one adult female T. to- strike position19. We defined interactions macrops in the core zone of SBR and two as direct if a viper came within half of a adult females in the transitional zone. All body length (or closer) to another viper, and three females were gravid during transmitter indirect if further but still visible on camera. implantation (n = 3, median SVL = 580 mm, Outcome of interactions were defined as range = 514 - 612; mass = 91.3 g, range = neutral, distracting, or agonistic. We classed 52.5 - 109, Table 1). Big- eyed pit vipers interactions as neutral when the focal viper exhibit profound sexual dimorphism did not appear to be aware of or did not (females being larger than males), with adult acknowledge a conspecific. The interaction males in our study area at mean mass was distracting when the focal viper precariously close to the 5% body mass appeared aware of or acknowledged a cutoff for transmitter implantation (they are conspecific, but no subsequent responses too small to ethically implant)15. To safely were evident. Agonistic outcomes included observe sex differences without unethically active responses, requiring subsequent implanting adult male vipers which were too movement, of a focal viper to a conspecific. small, we included an adult non-tracked 97 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER

FIGURE 1. Bushnell trail camera set to observe an ambushing big-eyed pit viper (Trimeresurus (Cryptelytrops) macrops).

We report median values for duration and minutes, for a median number of 2 bouts per occurrence of interactions. individual (Table 1). All interactions This research found that, in total, we occurred between early evening and early opportunistically set cameras (mean 8556.5 morning time (19:20 - 05:21) from late minutes per individual, n = 4, Table 1) on November to early May. and observed nine interactions between Females (n = 3) were observed interacting focal T. macrops and conspecifics for a total with other vipers for a total of 248 min for a of 272 minutes from May 2015- January median of 74 min per viper. All female 2017 (see at Movie Archives of interactions were at the low ground height Behavior (http://movspec.mus-nh.city.osaka. level (>0 - 0.5 m) except for one which was jp/ethol/title-e.php) and https://www.youtube. at groundstory height (0.5 - 1 m). Two of com/channel/UCdRlzXz9YbUR2eWyEAEG the three female T. macrops, one in the U4g). Median duration of each bout was 14 transition (TRMA220) and one in the core TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 98

TABLE 1. Summary of focal big- eyed pit viper (Trimeresurus (Cryptelytrops) macrops) biometrics (snout- vent length [SVL] in mm and mass in g), time observed on camera (in min), and number and duration (in min) of interactions observed. Locations are the same as Strine et al. (2018, “upper dam pond, shortened to “pond”) and Barnes et al. (2017, “canal”).

Biometrics Interactions Viper ID Location Sex SVL Mass Time observed Number Duration TRMA220 Canal Female 580 91.3 16307 4 28 TRMA226 Canal Male 424 24.2 7735 1 24 TRMA232 Canal Female 612 109.0 2254 1 74 TRMA271 Pond Female 514 52.5 7930 3 146

area (TRMA271), in this study interacted the day following the interaction. The male with conspecifics on multiple occasions returned to the same ambush site on the (median 3.5 interactions, median 7 min per night immediately following the agonistic interaction) within a short time frame for a interaction after the conspecific median of 70 min between interactions. The (presumably the same which disturbed him) single male (TRMA226) had a single had left its shelter and moved elsewhere observable interaction, for a total of 24 min, (not visible on camera). A conspecific at low ground level height (>0 - 0.5 m). appeared to chase a focal female off an Interactions of focal female vipers were ambush site in the core area (TRMA271) primarily indirect (6 bouts) rather than during an agonistic interaction. The focal direct (2 bouts). The most frequently viper completely abandoned the site (did not observed outcome of interactions with focal return, moved >5 m lateral distance to a female vipers was neutral (4 bouts), with new foraging site), while the conspecific distracting (2 bouts) and agonistic (2 bouts) immediately proceeded to forage at the outcomes infrequent. One female bout was ambush site previously occupied after the direct and agonistic in the transition area of focal female was out of sight on camera. SBR (TRMA220), and one was direct and In conclusion, novel findings of our agonistic in the core area of the reserve investigation include clear agonistic (TRMA271). The single focal male behavior between conspecifics which has (TRMA226) interaction was direct and not yet been recorded outside of a sexual agonistic. context (male combat) for green pit vipers Agonistic interactions (Fig. 2) varied in and insight into more frequently observed behavior following the encounters. One apathetic interactions. female in the transition area (TRMA220) Direct social interaction of green pit and the male (TRMA226) continued to vipers may be reduced due to largely ambush at the same sites following sedentary lifestyle. Green pit vipers are agonistic interactions for at least one night extremely sedentary and only the smallest afterwards. The viper which disturbed the viper in the world, the Namaqua dwarf male (TRMA226) appeared to shelter adder ( schneideri), displays smaller within close proximity (<0.5 m, observed known home range sizes among all entering and exiting on camera) of it during snakes12,19,20. How limited movement 99 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER

FIGURE 2. Agonistic interactions of three focal big-eyed pit vipers (Trimeresurus (Cryptelytrops) macrops) including female TRMA220 (A), male TRMA226 (B), and female TRMA271 (C) recorded on Bushnell trail cameras. Interacting vipers are circled in yellow for reference.

translates into social behavior remains behavior and reducing direct competition. largely unknown. Understanding of Sexual dimorphism, both in coloration and behavior and communication within in size, likely reduces competition and subpopulations is worth investigating with agonistic interactions15,21. Additionally, green pit vipers due to their small home several studies suggest niche partitioning ranges. Subpopulations which are naturally and vertical stratification among green pit or anthropogenically isolated from others vipers, including T. macrops15,21,22. These may show different behaviors or degrees of factors may explain the higher number of sociality. neutral interaction outcomes compared to Previous observations of big-eyed pit agonistic, and perhaps why we observed so viper morphology and natural history have few interactions overall. suggested unique adaptations for social TROPICAL NATURAL HISTORY. 20(1), APRIL 2020 100

Big-eyed pit vipers have been previously suggest they may display similar agonistic documented and suggested to breed characteristics at least occasionally (3 out of primarily between September and 9 interactions in our study) outside of the November, which corresponds to the end of breeding season. the rainy season in Thailand24,25. This We cautiously suggest limited resources species is unique among vipers in that biting and sub-optimal seasonal conditions may be has been directly observed in the wild driving factors behind the interactions we during male combat during the breeding witnessed on camera. Pit vipers in our study season, which has been suggested to be a interacted during the cold and hot dry period of increased agonistic behavior25. seasons, which were not optimal foraging Our observations (late November to early periods for anuran prey. Frogs likely May) occurred outside of previously comprise a significant portion of T. macrops reported mating season for the species. We diet24,33. Presence and utilization of quality describe the first evidence of social foraging sites may also be a premium during interactions in conspecific green pit vipers. these time periods (cold and hot dry Interactions primarily resulted in what seasons). Lateral distance between ambush appeared to be neutral outcomes, however, and shelter sites is negligible12,19, and the several interactions were clearly agonistic two are likely not independently related. which is novel for the green pit viper taxon Thus, site selection (and social behavior, outside of breeding activities. subsequently) is likely influenced by the Resource defense and territorial behavior balance of thermoregulation and energy likely evolved or occurs when the benefits expenditure to obtain additional nutrients. gained by defending a particular area that Shelter, resting, and ambush sites with contains required resources exceed the costs adequate prey abundance may be scarce in of defending it26,27,28. It is frequently rural communities and other highly observed in terrestrial vertebrate groups, disturbed areas, additionally increasing including birds, mammals, lizards, frogs, opportunities for interactions and and salamanders29,30; although evidence is competition. Decreased prey and increased scarce for snakes. Only two insular habitat homogeneity were observed for colubrids (Oligodon formosanus and timber rattlesnakes (C. horridus) in a rural Dinodon semicarinatum) defending sea landscape in North America, which turtle nests (food resource) against subsequently altered foraging behavior34. conspecifics have conclusively been Further investigation of ambush site suggested to display resource defense and selection, chemical cues, and prey territoriality among all known snake availability would greatly augment species31,32. Infrequent feeding and the behavioral inferences. Whether social unpredictability of exact time and place of interaction prevalence is related to ambush available prey were factors suggested by32 site availability or quality would be a as to why snakes generally do not defend beneficial testable hypothesis for future food resources. Not enough evidence was study. provided in our work to definitively From our camera observations, the characterize T. macrops as territorial by sex, conspecifics interacting with our focal season, or with increased human vipers appeared to be female T. macrops on disturbance; however, our observations the basis of size and general morphology, 101 BARNES ET AL. – SOCIAL BEHAVIOR DISPLAYED BY THE GREEN PIT VIPER

however, recording quality of the cameras subsequent communication and resulting was not sufficient to positively confirm behavior are crucial for ecological study and species, sex, or fecundity. Similarly, low conservation. recording rate (1-3 frames per minute) may indicate missed or misinterpreted behaviors. ACKNOWLEDGEMENTS Thus, we were conservative with our

characterizations of behaviors and outcomes We thank Suranaree University of of interactions, as we believe acknowledging Technology (SUT) for supporting this the limitations of camera technology is project. All methods were carried out under essential for reducing potential misinter- the guidelines and approval of the SUT pretation and overstating our results. animal use and ethics committee. The Similarly, we believe it is essential to not National Research Council of Thailand over-extrapolate our results due to our (NRCT), Thailand Institute of Scientific and limited sample size and having a single Technological Research (TISTR), and study area in northeast Thailand. Sakaerat Environmental Research Station While certainly a time intensive method, (SERS) provided funding, site permission, we encourage further study with fixed and logistical and technical support cameras to better understand the throughout the project. consequences of intra and interspecific

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